Fast and slow feedforward inhibitory circuits for cortical odor processing

Feedforward inhibitory circuits are key contributors to the complex interplay between excitation and inhibition in the brain. Little is known about the function of feedforward inhibition in the primary olfactory (piriform) cortex. Using in vivo two-photon-targeted patch clamping and calcium imaging...

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Main Authors: Norimitsu Suzuki, Malinda LS Tantirigama, K Phyu Aung, Helena HY Huang, John M Bekkers
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/73406
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author Norimitsu Suzuki
Malinda LS Tantirigama
K Phyu Aung
Helena HY Huang
John M Bekkers
author_facet Norimitsu Suzuki
Malinda LS Tantirigama
K Phyu Aung
Helena HY Huang
John M Bekkers
author_sort Norimitsu Suzuki
collection DOAJ
description Feedforward inhibitory circuits are key contributors to the complex interplay between excitation and inhibition in the brain. Little is known about the function of feedforward inhibition in the primary olfactory (piriform) cortex. Using in vivo two-photon-targeted patch clamping and calcium imaging in mice, we find that odors evoke strong excitation in two classes of interneurons – neurogliaform (NG) cells and horizontal (HZ) cells – that provide feedforward inhibition in layer 1 of the piriform cortex. NG cells fire much earlier than HZ cells following odor onset, a difference that can be attributed to the faster odor-driven excitatory synaptic drive that NG cells receive from the olfactory bulb. As a result, NG cells strongly but transiently inhibit odor-evoked excitation in layer 2 principal cells, whereas HZ cells provide more diffuse and prolonged feedforward inhibition. Our findings reveal unexpected complexity in the operation of inhibition in the piriform cortex.
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spelling doaj.art-8f2cb2613181442faa274c50a1f14d1e2022-12-22T02:02:04ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.73406Fast and slow feedforward inhibitory circuits for cortical odor processingNorimitsu Suzuki0https://orcid.org/0000-0002-9338-9099Malinda LS Tantirigama1https://orcid.org/0000-0003-0791-9389K Phyu Aung2https://orcid.org/0000-0003-3744-5321Helena HY Huang3https://orcid.org/0000-0002-1283-8586John M Bekkers4https://orcid.org/0000-0001-8619-5512Eccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, AustraliaEccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, Australia; Neurocure Center for Excellence, Charité Universitätsmedizin Berlin and Humboldt Universität, Berlin, GermanyEccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, AustraliaEccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, AustraliaEccles Institute of Neuroscience, John Curtin School of Medical Research, The Australian National University, Canberra, AustraliaFeedforward inhibitory circuits are key contributors to the complex interplay between excitation and inhibition in the brain. Little is known about the function of feedforward inhibition in the primary olfactory (piriform) cortex. Using in vivo two-photon-targeted patch clamping and calcium imaging in mice, we find that odors evoke strong excitation in two classes of interneurons – neurogliaform (NG) cells and horizontal (HZ) cells – that provide feedforward inhibition in layer 1 of the piriform cortex. NG cells fire much earlier than HZ cells following odor onset, a difference that can be attributed to the faster odor-driven excitatory synaptic drive that NG cells receive from the olfactory bulb. As a result, NG cells strongly but transiently inhibit odor-evoked excitation in layer 2 principal cells, whereas HZ cells provide more diffuse and prolonged feedforward inhibition. Our findings reveal unexpected complexity in the operation of inhibition in the piriform cortex.https://elifesciences.org/articles/73406piriform cortexinhibitionolfaction
spellingShingle Norimitsu Suzuki
Malinda LS Tantirigama
K Phyu Aung
Helena HY Huang
John M Bekkers
Fast and slow feedforward inhibitory circuits for cortical odor processing
eLife
piriform cortex
inhibition
olfaction
title Fast and slow feedforward inhibitory circuits for cortical odor processing
title_full Fast and slow feedforward inhibitory circuits for cortical odor processing
title_fullStr Fast and slow feedforward inhibitory circuits for cortical odor processing
title_full_unstemmed Fast and slow feedforward inhibitory circuits for cortical odor processing
title_short Fast and slow feedforward inhibitory circuits for cortical odor processing
title_sort fast and slow feedforward inhibitory circuits for cortical odor processing
topic piriform cortex
inhibition
olfaction
url https://elifesciences.org/articles/73406
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AT malindalstantirigama fastandslowfeedforwardinhibitorycircuitsforcorticalodorprocessing
AT kphyuaung fastandslowfeedforwardinhibitorycircuitsforcorticalodorprocessing
AT helenahyhuang fastandslowfeedforwardinhibitorycircuitsforcorticalodorprocessing
AT johnmbekkers fastandslowfeedforwardinhibitorycircuitsforcorticalodorprocessing